vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ19.574vavilov-2390Research ArticleГЕНОМИКА И ТРАНСКРИПТОМИКАPLANT GENETICS AND BREEDINGПластидный и митохондриальный геномы Vavilovia formosa (Stev.) Fed. и филогения родственных родов бобовыхThe plastid and mitochondrial genomes of Vavilovia Formosa (Stev.) Fed. and the phylogeny of related legume generaШацкаяН. В.ShatskayaN. V.

Новосибирск

Novosibirsk

БогдановаВ. С.BogdanovaV. S.

Новосибирск

Novosibirsk

https://orcid.org/0000-0001-5955-4057КостеринО. Э.KosterinO. E.

Новосибирск

Novosibirsk

kosterin@bionet.nsc.ruВасильевГ. В.VasilievG. V.

Новосибирск

Novosibirsk

КимеклисА. К.KimeklisA. K.

Пушкин, Санкт-Петербург

Pushkin, St. Petersburg

АндроновЕ. Е.AndronovE. E.

Пушкин, Санкт-Петербург

Pushkin, St. Petersburg

ПроворовН. А.ProvorovN. A.

Пушкин, Санкт-Петербург

Pushkin, St. Petersburg

Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics, SB RASRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университетРоссияInstitute of Cytology and Genetics, SB RAS; Novosibirsk State UniversityRussian FederationВсероссийский научно-исследовательский институт сельскохозяйственной микробиологииРоссияAll-Russia Research Institute for Agricultural MicrobiologyRussian Federation201908012020238972980Copyright © Шацкая Н.В., Богданова В.С., Костерин О.Э., Васильев Г.В., Кимеклис А.К., Андронов Е.Е., Проворов Н.А., 20202020Шацкая Н.В., Богданова В.С., Костерин О.Э., Васильев Г.В., Кимеклис А.К., Андронов Е.Е., Проворов Н.А.Shatskaya N.V., Bogdanova V.S., Kosterin O.E., Vasiliev G.V., Kimeklis A.K., Andronov E.E., Provorov N.A.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/2390

На основании данных высокопроизводительного секвенирования на платформах Illumina и PacBio тотальной ДНК, выделенной из образца Vavilovia formosa (Stev.) Fed. из Северной Осетии (Россия), собраны пластидный и митохондриальный геномы этого вида. Длинные риды, получаемые на платформе PacBio, оказались достаточными для надежной сборки геномов органелл, тогда как короткие риды, получаемые на платформе Illumina, – непригодными для этой цели ввиду значительной контаминации последовательностями ядерного происхождения. Геномы органелл представляют собой кольцевые молекулы ДНК, причем митохондриальный геном состоит из двух кольцевых хромосом. На основе имеющихся в публичных базах данных последовательностей пластидных геномов и пластидного генома Vavilovia предпринят филогенетический анализ, вовлекший некоторых представителей триб Fabeae, Trifolieae и Cicereae. Как и ожидалось, ветвь V. formosa оказалась сестринской к ветви Pisum L. (горох), а триба Fabeae – монофилетична. Позиция рода Trifolium L. (клевер) зависела от метода реконструкции филогении – он кластеризовался либо с Fabeae, либо с родами Medicago L. (люцерна), Trigonella L. (пажитник) и Melilotus Mill. (донник). Вне зависимости от метода реконструкции длина ветвей между последовательными дивергенциями была незначительной, что свидетельствует о быстрой радиации Trifolium, других представителей триб Trifolieae и Fabeae в течение короткого времени по сравнению с дальнейшей эволю цией соответствующих линий. Данные о родстве пластидных геномов рода Trifolium и трибы Fabeae коррелируют со сходством N2-фиксирующих симбионтов этих бобовых, представленных Rhizobium leguminosarum штаммов trifolii и viciae, тогда как симбионты Medicago, Melilotus и Trigonella принадлежат к видам Sinorhizobium meliloti и S. medicae, эволюционно отдаленным от Rhizobium.

The plastid and mitochondrial genomes of Vavilovia formosa (Stev.) Fed. were assembled on the base of the data of high-throughput sequencing of DNA isolated from a sample from North Osetia, Russia, using Illumina and PacBio platforms. The long PacBio reads were sufficient for reliable assembling organellar genomes while the short Illumina reads obtained from total DNA were unacceptable for this purpose because of substantial contamination by nuclear sequences. The organellar genomes were circular DNA molecules; the genome of mitochondria was represented by two circular chromosomes. A phylogenetic analysis on the basis of plastid genomes available in public databases was performed for some representatives of the tribes Fabeae, Trifolieae and Cicereae. As was expected, the V. formosa branch proved to be sister to the Pisum branch, and the tribe Fabeae was monophyletic. The position of Trifolium L. appeared sensitive to the phylogeny reconstruction method, either clustering with Fabeae or with the genera Medicago L., Trigonella L. and Melilotus Mill., but the internodes between successive divergences were short in all cases, suggesting that the radiation of Trifolium, other Trifolieae and Fabeae was fast, occurring within a small time interval as compared to further evolution of these lineages. The data on the relatedness of the plastid genomes of Trifolium and Fabeae correlate with the similarity of N2-fixing symbionts in these legumes represented by Rhizobium leguminosarum biovars trifolii and viciae, while the symbionts of Medicago, Melilotus and Trigonella belong to the Sinorhizobium meliloti and S. medicae species, which are distant from Rhizobium.

Vavilovia Formosa (Stev.) Fed.Vavilovia A. FedorovLathyrus L.Vicia L.Pisum L.Lens L.Trifolium L.Medicago L.Trigonella L.Melilotus Mill.Cicer L.FabeaeTrifolieaeCicereaeдикие сородичи культурных растенийгорохпластидный геномфилогенияпарафилиямонофилияVavilovia formosa (Stev.) Fed.Vavilovia A. FedorovLathyrus L.Vicia L.Pisum L.Lens L.Trifolium L.Medicago L.Trigonella L.Melilotus Mill.Cicer L.FabeaeTrifolieaeCicereaecrop wild relativespeaplastid genomephylogenyparaphylymonophylyThe work by N.V. Shatskaya, V.S. Bogdanova, O.E. Kosterin and G.V. Vasiliev on the assembly of the plastid and mitochondrial genomes and phylogenetic analysis was supported by State Budgeted Project 0324-2019-0041 for the Institute of Cytology and Genetics SB RAS, Novosibirsk, and the Russian Foundation for Basic Research, project 19-04-00162. The work by E.A. Andronov, A.K. Kimeklis, and N.A. Provorov on DNA isolation and high-throughput sequencing was supported by the Russian Science Foundation, project 19-16-00081. The assembly of organellar genomes and phylogenetic analysis were performed with the use of the Computational Facility of the Siberian Supercomputer Center SB RAS and the Computational Facility of the Novosibirsk State University.The work by N.V. Shatskaya, V.S. Bogdanova, O.E. Kosterin and G.V. Vasiliev on the assembly of the plastid and mitochondrial genomes and phylogenetic analysis was supported by State Budgeted Project 0324-2019-0041 for the Institute of Cytology and Genetics SB RAS, Novosibirsk, and the Russian Foundation for Basic Research, project 19-04-00162. The work by E.A. Andronov, A.K. Kimeklis, and N.A. Provorov on DNA isolation and high-throughput sequencing was supported by the Russian Science Foundation, project 19-16-00081. The assembly of organellar genomes and phylogenetic analysis were performed with the use of the Computational Facility of the Siberian Supercomputer Center SB RAS and the Computational Facility of the Novosibirsk State University.ReferencesAkopian J.A., Gabrielyan I.G. On high­mountain pea, Vavilovia formosa (Stev.) Fed. (Fabaceae) in Armenia. Crop Wild Relative. 2008;6: 26­27.Akopian J.A., Gabrielyan I.G. On high­mountain pea, Vavilovia formosa (Stev.) Fed. (Fabaceae) in Armenia. Crop Wild Relative. 2008;6: 26­27.Akopian J., Sarukhanyan N., Gabrielyan I., Vanyan A., Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Ambrose M. Reports on establishing an ex situ site for ‘‘beautiful’’ vavilovia (Vavilovia formosa) in Armenia. Genet. Resour. Crop Evol. 2010;57:1127­1134. DOI 10.1007/s10722­010­9606­0.Akopian J., Sarukhanyan N., Gabrielyan I., Vanyan A., Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Ambrose M. Reports on establishing an ex situ site for ‘‘beautiful’’ vavilovia (Vavilovia formosa) in Armenia. Genet. Resour. Crop Evol. 2010;57:1127­1134. DOI 10.1007/s10722­010­9606­0.Akopian J.A., Sinjushin A.A., Gabrielyan I.G., Shaboyan G. On some biomorphological peculiarities of seedlings of Vavilovia formosa (Stev.) Fed. (Fabaceae). Legum Perspect. 2014;5:34­35.Akopian J.A., Sinjushin A.A., Gabrielyan I.G., Shaboyan G. On some biomorphological peculiarities of seedlings of Vavilovia formosa (Stev.) Fed. (Fabaceae). Legum Perspect. 2014;5:34­35.Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403­410. DOI 10.1016/S0022­2836(05)80360­2.Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403­410. DOI 10.1016/S0022­2836(05)80360­2.Atlagić J., Mikić A., Sarukhanyan N., Vanyan A., Akopian J., Gabrielyan I., Smýkal P., Kenicer G., Vishnyakova M. Ambrose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). II. Morphology of androecium and gynoecium and mitosis. Pisum Genet. 2010;41:21­24.Atlagić J., Mikić A., Sarukhanyan N., Vanyan A., Akopian J., Gabrielyan I., Smýkal P., Kenicer G., Vishnyakova M. Ambrose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). II. Morphology of androecium and gynoecium and mitosis. Pisum Genet. 2010;41:21­24.Biondi E.G., Giuntini P.E., Roumiantseva M.L., Andronov E.E., Onichtchouk O.P., Kurchak O.N., Simarov B.V., Dzyubenko N.I., Mengoni A., Bazzicalupo M. Genetic relationship of Sinorhizobium meliloti and Sinorhizobium medicae strains isolated from Caucasian region. FEMS Microbiol. Lett. 2003;220(2):207­213. DOI 10.1016/S0378­1097(03)00098­3.Biondi E.G., Giuntini P.E., Roumiantseva M.L., Andronov E.E., Onichtchouk O.P., Kurchak O.N., Simarov B.V., Dzyubenko N.I., Mengoni A., Bazzicalupo M. Genetic relationship of Sinorhizobium meliloti and Sinorhizobium medicae strains isolated from Caucasian region. FEMS Microbiol. Lett. 2003;220(2):207­213. DOI 10.1016/S0378­1097(03)00098­3.Chevreux B., Wetter T., Suhai S. Genome sequence assembly using trace signals and additional sequence information. In: Computer Science and Biology: Proc. German Conference on Bioinformatics (GCB). 1999;99:45­56.Chevreux B., Wetter T., Suhai S. Genome sequence assembly using trace signals and additional sequence information. In: Computer Science and Biology: Proc. German Conference on Bioinformatics (GCB). 1999;99:45­56.Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012; 9(8):772. DOI 10.1038/nmeth.2109.Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012; 9(8):772. DOI 10.1038/nmeth.2109.Davis P.H. Vavilovia A. Fed. In: Davis P.H. (Ed.) Flora of Turkey and East Aegean Islands, Vol. 3. Royal Botanical Gardens Edinburgh, Edinburgh. 1970;44­45.Davis P.H. Vavilovia A. Fed. In: Davis P.H. (Ed.) Flora of Turkey and East Aegean Islands, Vol. 3. Royal Botanical Gardens Edinburgh, Edinburgh. 1970;44­45.de la Peña T.C., Fedorova E., Pueyo J.J., Lucas M.M. The symbiosome: legume and rhizobia co­evolution toward a nitrogen­fixing organelle? Front. Plant Sci. 2018;8:2229. DOI 10.3389/fpls.2017.02229.de la Peña T.C., Fedorova E., Pueyo J.J., Lucas M.M. The symbiosome: legume and rhizobia co­evolution toward a nitrogen­fixing organelle? Front. Plant Sci. 2018;8:2229. DOI 10.3389/fpls.2017.02229.Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007;7:1. DOI 10.1186/1471­2148­7­214.Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007;7:1. DOI 10.1186/1471­2148­7­214.Dudeja S.S., Nidhi. Molecular diversity of rhizobia and nonrhizobia bacteria from nodules of cool season legumes. In: Salar R.K., Gahlawat S.K., Siwach P., Duhan J.S. (Eds.). Biotechnology: Prospects and Application. New Dehli: Springer, India, 2013;113­125. DOI 10.1007/978­81­322­1683­4_10.Dudeja S.S., Nidhi. Molecular diversity of rhizobia and nonrhizobia bacteria from nodules of cool season legumes. In: Salar R.K., Gahlawat S.K., Siwach P., Duhan J.S. (Eds.). Biotechnology: Prospects and Application. New Dehli: Springer, India, 2013;113­125. DOI 10.1007/978­81­322­1683­4_10.Gnerre S., Maccallum I., Przybylski D., Ribeiro F.J., Burton J.N., Wal ker B.J., Sharpe T., Hall G., Shea T.P., Sykes S., Berlin A.M., Aird D., Costello M., Daza R., Williams L., Nicol R., Gnirke A., Nusbaum C., Lander E.S., Jaffe D.B. High­quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. USA. 2011;108:1513­1508. DOI 10.1073/pnas.1017351108.Gnerre S., Maccallum I., Przybylski D., Ribeiro F.J., Burton J.N., Wal ker B.J., Sharpe T., Hall G., Shea T.P., Sykes S., Berlin A.M., Aird D., Costello M., Daza R., Williams L., Nicol R., Gnirke A., Nusbaum C., Lander E.S., Jaffe D.B. High­quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl. Acad. Sci. USA. 2011;108:1513­1508. DOI 10.1073/pnas.1017351108.Gualberto J.M., Mileshina D., Wallet C., Niazi A.K., Weber­Lotfi F., Dietrich A. The plant mitochondrial genome: dynamics and maintenance. Biochimie. 2014;100:107­120. DOI 10.1016/j.biochi.2013. 09.016. PMID: 24075874.Gualberto J.M., Mileshina D., Wallet C., Niazi A.K., Weber­Lotfi F., Dietrich A. The plant mitochondrial genome: dynamics and maintenance. Biochimie. 2014;100:107­120. DOI 10.1016/j.biochi.2013. 09.016. PMID: 24075874.Guindon S., Gascuel O. A simple, fast and accurate method to estimate large phylogenies by maximum­likelihood. Syst. Biol. 2003;52: 696­704. DOI 10.1080/10635150390235520.Guindon S., Gascuel O. A simple, fast and accurate method to estimate large phylogenies by maximum­likelihood. Syst. Biol. 2003;52: 696­704. DOI 10.1080/10635150390235520.Kreplak K., Madoui M.­A., Cápal P., Novák P., Labadie K., Aubert G., Bayer P.E., Gali K.K., Syme R.A., Main D., Klein A., Bérard A., Vrbová I., Fournier C., d´Agata L., Belser C., Berrabah W., Toegelová H., Milec Z., Vrána J., Lee H., Kougbeadjo A., Térézol M., Huneau C., Turo C.J., Mohellibi N., Neumann P., Falque M., Gallardo K., McGee R., Tar’an B., Bendahmane A., Aury J.M., Batley J., Le Paslier M.C., Ellis N., Warkentin T.D., Coyne C.J., Salse J., Edwards D., Lichtenzveig J., Macas J., Doležel J., Wincker P., Burstin J. A reference genome for pea provides insight into legume genome evolution. Nat. Genet. 2019;51:1411­1422. DOI 10.1038/s41588­019­0480­1.Kreplak K., Madoui M.­A., Cápal P., Novák P., Labadie K., Aubert G., Bayer P.E., Gali K.K., Syme R.A., Main D., Klein A., Bérard A., Vrbová I., Fournier C., d´Agata L., Belser C., Berrabah W., Toegelová H., Milec Z., Vrána J., Lee H., Kougbeadjo A., Térézol M., Huneau C., Turo C.J., Mohellibi N., Neumann P., Falque M., Gallardo K., McGee R., Tar’an B., Bendahmane A., Aury J.M., Batley J., Le Paslier M.C., Ellis N., Warkentin T.D., Coyne C.J., Salse J., Edwards D., Lichtenzveig J., Macas J., Doležel J., Wincker P., Burstin J. A reference genome for pea provides insight into legume genome evolution. Nat. Genet. 2019;51:1411­1422. DOI 10.1038/s41588­019­0480­1.Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947­2948. DOI 10.1093/bioinformatics/btm404.Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947­2948. DOI 10.1093/bioinformatics/btm404.Lohse M., Drechsel O., Kahlau S., Bock R. OrganellarGenomeDRAW – a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013;41(Web Server issue):W575­W581. DOI 10.1093/nar/gkt289.Lohse M., Drechsel O., Kahlau S., Bock R. OrganellarGenomeDRAW – a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013;41(Web Server issue):W575­W581. DOI 10.1093/nar/gkt289.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Akopian J., Sarukha nyan N., Gabrielyan I., Vanyan A., Toker C., Ćupina B., Ambrose M., Mihailović V., Ellis N. A revival of the research on beautiful vavilovia (Vavilovia formosa syn. Pisum formosum). Pisum Genet. 2009;41:34­39.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Akopian J., Sarukha nyan N., Gabrielyan I., Vanyan A., Toker C., Ćupina B., Ambrose M., Mihailović V., Ellis N. A revival of the research on beautiful vavilovia (Vavilovia formosa syn. Pisum formosum). Pisum Genet. 2009;41:34­39.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Sarukhanyan N., Akopian J., Vanyan A., Gabrielyan I., Smýkalová I., Sherbakova E., Zorić L., Atlagić J., Škorić T., Cupina B., Krstić Р., Jajić I., Antanasović S., Dorđević V., Mihailović V., Ivanov A., Ochatt S., Ambrose M. The bicentenary of the research on ‘beautiful’ Vavilovia (Vavilovia formosa), a legume crop wild relative with taxonomic and agronomic potential. Bot. J. Linn. Soc. 2013;172:524­531. DOI 10.1111/boj.12060.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Sarukhanyan N., Akopian J., Vanyan A., Gabrielyan I., Smýkalová I., Sherbakova E., Zorić L., Atlagić J., Škorić T., Cupina B., Krstić Р., Jajić I., Antanasović S., Dorđević V., Mihailović V., Ivanov A., Ochatt S., Ambrose M. The bicentenary of the research on ‘beautiful’ Vavilovia (Vavilovia formosa), a legume crop wild relative with taxonomic and agronomic potential. Bot. J. Linn. Soc. 2013;172:524­531. DOI 10.1111/boj.12060.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Sarukhanyan N., Akopian J.A., Vanyan A., Gabrielyan I., Smýkalová I., Sherbakova E., Zorić L., Atlagić J., Zeremski­Škorić T., Cupina B., Krstić Р., Jajić I., Antanasović S., Dorđević V., Mihailović V., Ivanov A., Ochatt S., Toker C., Zlatković B., Ambrose M. Beauty will save the world, but will the world save beauty? The case of the highly endangered Vavilovia formosa (Stev.). Fed. Planta. 2014;240(5):1139­1146. DOI 10.1007/s00425­014­2136­9.Mikić A., Smýkal P., Kenicer G., Vishnyakova M., Sarukhanyan N., Akopian J.A., Vanyan A., Gabrielyan I., Smýkalová I., Sherbakova E., Zorić L., Atlagić J., Zeremski­Škorić T., Cupina B., Krstić Р., Jajić I., Antanasović S., Dorđević V., Mihailović V., Ivanov A., Ochatt S., Toker C., Zlatković B., Ambrose M. Beauty will save the world, but will the world save beauty? The case of the highly endangered Vavilovia formosa (Stev.). Fed. Planta. 2014;240(5):1139­1146. DOI 10.1007/s00425­014­2136­9.Oskoueiyan R., Kazempour­Osaloo S., Maassoumi A.A., Nejadsattari T., Mozaffarian V. Phylogenetic status of Vavilovia formosa (Fabaceae­Fabeae) based on nrDNA ITS and cpDNA sequences. Biochem. Syst. Ecol. 2010;38:313­319. DOI 10.1016/j.bse.2010.01.011.Oskoueiyan R., Kazempour­Osaloo S., Maassoumi A.A., Nejadsattari T., Mozaffarian V. Phylogenetic status of Vavilovia formosa (Fabaceae­Fabeae) based on nrDNA ITS and cpDNA sequences. Biochem. Syst. Ecol. 2010;38:313­319. DOI 10.1016/j.bse.2010.01.011.Safronova V.I., Kimeklis A.K., Chizhevskaya E.P., Belimov A.A., Andronov E.E., Pinaev A.G., Tikhonovich I.A., Pukhaev A.R., Popov K.P. Genetic diversity of rhizobia isolated from nodules of the relic species Vavilovia formosa (Stev.) Fed. Antonie van Leeuwenhoek. 2014;105:389­399. DOI 10.1007/s10482­013­0089­9.Safronova V.I., Kimeklis A.K., Chizhevskaya E.P., Belimov A.A., Andronov E.E., Pinaev A.G., Tikhonovich I.A., Pukhaev A.R., Popov K.P. Genetic diversity of rhizobia isolated from nodules of the relic species Vavilovia formosa (Stev.) Fed. Antonie van Leeuwenhoek. 2014;105:389­399. DOI 10.1007/s10482­013­0089­9.Safronova V.I., Kuznetsova I.G., Sazanova A.L., Kimeklis A.K., Belimov A.A., Andronov E.E., Pinaev A.G., Chizhevskaya E.P., Pukhaev A.R., Popov K.P., Willems A., Tikhonovich I.A. Bosea vaviloviae sp. nov., a new species of slow­growing rhizobia isolated from nodules of the relict species Vavilovia formosa (Stev.) Fed. Antonie van Leeuwenhoek. 2015;107:911­920. DOI 10.1007/s10482­015­0383­9.Safronova V.I., Kuznetsova I.G., Sazanova A.L., Kimeklis A.K., Belimov A.A., Andronov E.E., Pinaev A.G., Chizhevskaya E.P., Pukhaev A.R., Popov K.P., Willems A., Tikhonovich I.A. Bosea vaviloviae sp. nov., a new species of slow­growing rhizobia isolated from nodules of the relict species Vavilovia formosa (Stev.) Fed. Antonie van Leeuwenhoek. 2015;107:911­920. DOI 10.1007/s10482­015­0383­9.Schaefer H., Hechenleitner P., Santos­Guerra A., Menezes de Sequeira M., Pennington R.T., Kenicer G., Carine M.A. Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle­Atlantic island lineages. BMC Evol. Biol. 2012;12:250. DOI 10.1186/1471­2148­12­250.Schaefer H., Hechenleitner P., Santos­Guerra A., Menezes de Sequeira M., Pennington R.T., Kenicer G., Carine M.A. Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle­Atlantic island lineages. BMC Evol. Biol. 2012;12:250. DOI 10.1186/1471­2148­12­250.Sinjushin A.A., Belyakova A.S. On intraspecific variation of Vavilovia formosa (Stev.) Fed. (= Pisum formosum (Stev.) Alef.: Fabeae). Pisum Genet. 2010;41:31­34.Sinjushin A.A., Belyakova A.S. On intraspecific variation of Vavilovia formosa (Stev.) Fed. (= Pisum formosum (Stev.) Alef.: Fabeae). Pisum Genet. 2010;41:31­34.Sinjushin A.A., Demidenko N.V., Gostimskii S.A. Preliminary report on taxonomical position of Vavilovia formosa (Stev.) Fed. evidenced from morphological and molecular data. Pisum Genet. 2009;41: 15­20.Sinjushin A.A., Demidenko N.V., Gostimskii S.A. Preliminary report on taxonomical position of Vavilovia formosa (Stev.) Fed. evidenced from morphological and molecular data. Pisum Genet. 2009;41: 15­20.Sloan D.B., Alverson A.J., Chuckalovcak J.P., Wu M., McCauley D.E., Palmer J.D., Taylor D.R. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012;10(1):e1001241. DOI 10.1371/journal.pbio.100124.Sloan D.B., Alverson A.J., Chuckalovcak J.P., Wu M., McCauley D.E., Palmer J.D., Taylor D.R. Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012;10(1):e1001241. DOI 10.1371/journal.pbio.100124.Smith D.R., Keeling P.J. Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc. Natl. Acad. Sci. USA. 2015;112:10177­10184. DOI 10.1073/pnas.1422049112.Smith D.R., Keeling P.J. Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc. Natl. Acad. Sci. USA. 2015;112:10177­10184. DOI 10.1073/pnas.1422049112.Tamura K., Stecher G., Peterson D., Kumar S. MEGA6: molecular evolutionary genetics analysisversion 6.0. Mol. Biol. Evol. 2013;30: 2725­2729. DOI 10.1093/molbev/mst197.Tamura K., Stecher G., Peterson D., Kumar S. MEGA6: molecular evolutionary genetics analysisversion 6.0. Mol. Biol. Evol. 2013;30: 2725­2729. DOI 10.1093/molbev/mst197.Vishnyakova M., Burlyaeva M., Akopian J., Murtazaliev R., Mikić A. Reviewing and updating the detected locations of beautiful vavilovia (Vavilovia formosa) on the Caucasus sensu stricto. Genet. Res. Crop Evol. 2016;63:1085­1102. DOI 10.1007/s10722­016­0440­x.Vishnyakova M., Burlyaeva M., Akopian J., Murtazaliev R., Mikić A. Reviewing and updating the detected locations of beautiful vavilovia (Vavilovia formosa) on the Caucasus sensu stricto. Genet. Res. Crop Evol. 2016;63:1085­1102. DOI 10.1007/s10722­016­0440­x.Vishnyakova M.A., Burlyaeva M.O., Seferova I.V., Bagmet L.V., Semenov V.A. Expedition collections of the tribe Vicieae representatives in the Russian Federation and the adjacent territories of the North Caucasus. Bull. Appl. Bot. Genet. Plant Breed. 2013;172: 82­86.Vishnyakova M.A., Burlyaeva M.O., Seferova I.V., Bagmet L.V., Semenov V.A. Expedition collections of the tribe Vicieae representatives in the Russian Federation and the adjacent territories of the North Caucasus. Bull. Appl. Bot. Genet. Plant Breed. 2013;172: 82­86.Wojciechowski M.F., Lavin M., Sanderson M.J. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well­supported subclades within the family. Am. J. Bot. 2004;91(11):1846­1862. DOI 10.3732/ajb.91.11.1846.Wojciechowski M.F., Lavin M., Sanderson M.J. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well­supported subclades within the family. Am. J. Bot. 2004;91(11):1846­1862. DOI 10.3732/ajb.91.11.1846.Yakovlev G.P. Bobovye Zemnogo Shara = Legumes of the Globe. Leningrad: Nauka Publ., 1991. (in Russian)Yakovlev G.P. Bobovye Zemnogo Shara = Legumes of the Globe. Leningrad: Nauka Publ., 1991. (in Russian)Zemerski­Škorić T., Mikić A., Sarukhanyan N., Vanyan A., Akopian J., Gabrielyan I., Smýkal P., Kenicer G., Vishnyakova M., A m brose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). III. Contents of macroand microelements. Pisum Genet. 2010;41:28­30.Zemerski­Škorić T., Mikić A., Sarukhanyan N., Vanyan A., Akopian J., Gabrielyan I., Smýkal P., Kenicer G., Vishnyakova M., A m brose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). III. Contents of macroand microelements. Pisum Genet. 2010;41:28­30.Zorić L., Luković J., Mikić A., Akopian J., Gabrielyan I., Sarukhanyan N., Vanyan A., Smýkal P., Kenicer G., Vishnyakova M., Ambrose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). I. Anatomy of stem, leaf and calyx. Pisum Genet. 2010;41:21­24.Zorić L., Luković J., Mikić A., Akopian J., Gabrielyan I., Sarukhanyan N., Vanyan A., Smýkal P., Kenicer G., Vishnyakova M., Ambrose M. Contributions to the characterization of Vavilovia formosa (syn. Pisum formosum). I. Anatomy of stem, leaf and calyx. Pisum Genet. 2010;41:21­24.

The authors declare that there are no conflicts of interest present.